Phylogenetic and functional structures of plant

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Article details Cui YC Song K Guo XY Bodegom PM van Pan YJ Tian ZH Chen XS Wang J amp Da LJ (2019) Phylogenetic and functional structures of plant communities along a spatiotemporal urbanization gradient effects of colonization and extinction Journal of Vegetation Science 30(2) 341-351 Doi 101111jvs12724

J Veg Sci 201930341ndash351 wileyonlinelibrarycomjournaljvs emsp|emsp341

Journal of Vegetation Science

copy 2019 International Association for Vegetation Science

Received7February2018emsp |emsp Revised3December2018emsp |emsp Accepted20December2018DOI101111jvs12724

R E S E A R C H A R T I C L E

Phylogenetic and functional structures of plant communities along a spatiotemporal urbanization gradient Effects of colonization and extinction

Yi Chong Cui12 emsp| Kun Song12 emsp| Xue Yan Guo12emsp| Peter M van Bodegom3 emsp| Ying Ji Pan3 emsp| Zhi Hui Tian4emsp| Xiao Shuang Chen5emsp| Jie Wang12emsp| Liang Jun Da12

1Shanghai Key Lab for Urban Ecological ProcessesandEco-RestorationSchoolofEcologicalandEnvironmentalSciencesEastChinaNormalUniversityShanghaiChina2InstituteofEco-ChongmingShanghaiChina3InstituteofEnvironmentalSciences(CML)LeidenUniversityLeidenTheNetherlands4Eco-EnvironmentalProtectionResearchInstituteShanghaiAcademyofAgriculturalSciencesShanghaiChina5CollegeofMaterialsScienceandEngineeringDonghuaUniversityShanghaiChina

CorrespondenceKunSongandLiangJunDaShanghaiKeyLab for Urban Ecological Processes and Eco-RestorationSchoolofEcologicalandEnvironmentalSciencesEastChinaNormalUniversityShanghaiChinaEmails ksongdesecnueducn ljdadesecnueducn

Funding information ThisworkwassupportedbytheNationalNaturalScienceFoundationofChina(projectNo31770468)SpecialFoundationforStateMajor Basic Research Program of China (2015FY210200-4)ScienceandTechnologyCommissionofShanghaiMunicipality(18DZ120460018295810400)

Co-ordinatingEditorIngolfKuumlhn

AbstractQuestion Urbanizationhasremarkableimpactsonthephylogeneticandfunctionalstructuresofplant communitiesBoth temporal and spatial comparisonsalongur-banizationgradientsarewidelyusedinrelatedstudiesbuttherehasbeenalackofconsistencyintheresultsMoreoverthereisaneedforstudiesthatdeterminespe-ciesassemblymechanismsthroughimmigrationandextinctionThereforetwoques-tions were addressed (a) How do the phylogenetic and functional structures ofruderalspeciesrespondtourbanizationanddotheirshiftsfollowasimilarpatternalongtemporalandspatialurbanizationgradients(b)Whatarethekeyunderlyingprocesses ieeitherextinction-orcolonization-causedclustering thatdeterminethephylogeneticandfunctionalstructuresofruderalspeciesunderurbanizationStudy site Twometropoles(ShanghaiandHarbin)experiencingrapidurbanizationinChinaMethods Wecollectedoccurrencedataonruderalspeciesfrom1955andthepresentintwocitiesStandardizedeffectsizesofmeanpairwisephylogeneticdistanceandofmeanpairwisefunctionaldistancevalues(MPDSESandMFDSESresp)werecalculatedtotestwhethertherewasphylogeneticandorfunctionalstructureclusteringalongspatialortemporalurbanizationgradientsβ-MPDSES and β-MFDSES values were used toquantifythesimilaritiesamongcolonistsextinctspeciesandresidentsResults AlongboththespatialandtemporalgradientstheMPDSES values in each citydecreasedfromsignificantlypositivetosignificantlynegativewithincreasingur-banizationInconsistentlyalongthetemporalgradientstheβ-MPDSESvaluesofthecolonistsextinctspeciestotheresidentsweresignificantlynegativealongthespa-tialgradientstheβ-MPDSESvaluesofextinctspeciestoresidentsweresignificantlypositivewithincreasingurbanizationConclusions Wefoundtherewasaclearphylogeneticclusteringofruderalspecieswith increasing spatial and temporal urbanization gradients Our analysis showedthatthechangesacrosstheurbanndashruralgradientaremainlydrivenbyspeciesgoingextinct that are phylogenetically dissimilar to the resident species The temporal

342emsp |emsp emspenspJournal of Vegetation Science

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1emsp |emspINTRODUC TION

Changes in human-influenced landscape structure and in speciesmigrationhavearemarkableimpactonnaturalspeciescompositionworldwide (Collingham amp Huntley 2000 HilleRisLambers 2015KeshtkarampVoigt 2016VitousekMooney LubchenkoampMelillo1997) One of the core anthropogenic activities responsible forthesechangesisurbanization(Hautieretal2015Ivesetal2016McKinney 2002 2008) heavily modifying the local environmenttosuithumanneedsanddesires(Palmaetal2017)Fifty-fourper-centoftheworldpopulationlivedinurbanareasin2015andthiswillincreasecontinuallyandrapidlyto60by2030(WorldHealthOrganizationampUN-Habitat2016)

Thedensepopulationandintensiveindustrialandtransportationactivities in urban areas have causedhabitat loss and fragmentedlandscapestructuresinlocalecosystems(CurritampEasterling2009Mack amp Lonsdale 2001 McDonnell etal 1997 Price DorcasGallantKlaverampWillson2006)Moreovernumerousexoticplantspecieshavecolonizedurbanregionsthroughglobaltradeandgar-deningpractices(Boivinetal2016Hopeetal2003)Suchtran-sitionsmayaffectnotonlythetaxonomiccompositionbutalsothephylogeneticandfunctionalpatternsofplantcommunities(Čeplovaacuteetal2015JohnsonTauzerampSwan2015KnappKuumlhnSchweigerampKlotz2008KnappKuumlhnStolleampKlotz2010KnappWinterampKlotz2017Pianoetal2016)

Theeffectsofurbanizationonplant communitypatternshavegenerally been studied using temporal comparison approaches(beforendashafter urbanization gradients) and spatial comparison ap-proaches (urbanndashrural gradients) The latter can be considered tobe a space-for-time substitutionmethod So far empirical studieshaveusedspatialcomparisonbecauseofthedifficultyinobtaininghistoricalplantdataandindicatethatthephylogeneticdiversityofplantspeciesdecreaseswithincreasingspatialurbanization(Breza2015Johnsonetal2015Knappetal2012)Furthermoreithasbeenreportedthaturbanizationfavorsnativeandnon-nativespon-taneousspecieswithdisturbance-toleranttraitsieruderalspecies(includingweedsandgrasses)inurbanecosystemsandalsoleadstoachange in thephylogeneticand functional structuresof speciesaswell(Duncanetal2011Palmaetal2017RicottaGodefroidHeathfield amp Mazzoleni 2015 Ricotta Heathfield Godefroid ampMazzoleni 2012)However few studies have explicitly addressedthedynamiceffectsoftemporalurbanizationonplantcommunitiesDuetothelimitedgrowthratesorresilienceofspeciestheresponses

ofplantspeciestothehabitatchangesaretime-laggedastheresultof dynamic processes over long periods and the spatial patternsof plant species under urbanization could be biased (BonthouxBarnagaud Goulard amp Balent 2013) It has been suggested thatspace-for-timesubstitutionsmightignoretheactualdynamiceffectsofurbandevelopmentandlandscapechangesovertimebutoveres-timatethevariationduetospatialheterogeneity(AdlerampLauenroth2003Bonthouxetal2013FukamiampWardle2005)Thusthereisaneedforstudiessimultaneouslyapplyingtimeseriesandspatialcomparisonapproachestoanalyzetheinducedbiases

Phylogeneticandfunctionalstructuresdepictspeciesrsquoevolution-aryhistoriesandmechanismsofspeciesassemblymediatedthroughenvironmental stressors and species interactions (Chave Chustamp Theacutebaud 2007 Diacuteaz amp Cabido 2001McGill EnquistWeiherampWestoby 2006) Greater phylogeneticfunctional diversity andhealthierstructuresleadtoahigherecosystemstability(Knappetal2017)Studyingtheresponsesofphylogeneticandfunctionalstruc-turetourbanizationwillnotonlyguideustoconserveoururbanna-turebutwillalsoofferdeepinsightsintothemechanismsunderlyinghowurbanizationaffectsplantbiodiversityFor instanceenviron-mentalfilterscouldclusterthephylogeneticstructureofspeciesandselectsimilarfunctionaltraitsbypreventingthepersistenceofun-suitablespeciesinaparticularhabitatAsanabiotic-environmentalfilterdisturbanceregimestendtocausephylogeneticandfunctionalclusteringinplantcommunities(BrunbjergBorchseniusEiserhardtEjrnaeligsampSvenning2012Čeplovaacuteetal 2015) In contrast com-petitiveexclusioncandispersespeciesrsquophylogeneticandfunctionalstructures by limiting the coexistence of closely related speciesthroughintensecompetitionjustasDarwinsnaturalizationhypoth-esisclaims(YannelliKochJeschkeampKollmann2017)Meanwhilecurrentstudies indicatethatcompetitiveexclusionmightalso leadtophylogeneticandorfunctionalclusteringbyexcludinggroupsofecologicallysimilarspecieswithlowcompetitiveabilities(MayfieldampLevine2010)Inthiscasespecieswithlowercompetitiveabilitiesareexcludedby the strongeroneswhich should causedissimilar-ity infunctionaltraitsamongthespeciesthatbecomeextinctandresidents

Recentlyinordertodistinguishtheeffectsofimmigrationandlocalextinctionprocessesonplantcommunitiesanewanalyticalstrategywasproposedinastudyonphylogeneticandfunctionalchanges over community succession by comparing the phyloge-neticandfunctionalsimilaritiesamongcolonistsandextinctandresidentspecies(Lietal2015)Ifphylogeneticclusteringoccurs

dynamicsarehoweverprimarilydrivenbycolonistspeciesthatarephylogeneticallysimilartotheresidentspecies

K E Y W O R D S

colonistsextinctioninvasivespeciesruderalspeciesspace-for-timesubstitutionurbanplantcommunity

emspensp emsp | emsp343Journal of Vegetation Science

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thismaybeduetothelocalextinctionofspeciesthatarephyloge-neticallyandfunctionallydissimilartotheresidentsorduetothecolonizationofspeciesthatarephylogeneticallyandfunctionallysimilar to the residents (Li etal 2015) Likewiseoverdispersioncouldbedrivenbytheextinctionofspeciesthatarephylogenet-icallyandfunctionallysimilartotheresidentsorbythecoloniza-tionofspeciesthatarephylogeneticallyandfunctionallydissimilartotheresidents(Figure1)Hencedistinguishingthecontributionsofcolonizationandextinctiontothechangesinphylogeneticandfunctionalstructuresinurbanizationcouldrevealthekeyunderly-ingmechanismthatrulesspeciesassemblyinurbanareas

As spontaneous plants in urban area ruderal plant specieshavehighsensitivityandashort lifecycleandthuscanrespondtotheurbanhabitatheterogeneityandrapidlyadapttothehab-itats by changing their morphology physiology and behaviorThus ruderal species are theoptimally indicators forurbaniza-tion(ChenWangLiangLiuampDa2014TianSongampDa2015)Inthisstudyweanalyzedthephylogeneticandfunctionalstruc-turesofruderalplantspeciesintwoChinesecitiesandevaluatedthe differences among colonistsextinct species and residentsusingtimeseries(beforendashafterurbanization)andspatialcompari-sonapproaches(urbanndashruralurbanizationgradients)Weaimedtorevealtheresponsesofruderalphylogeneticandfunctionalstruc-turestourbanizationandtospecificallyanswerthefollowingtwoquestions

1 How do the phylogenetic and functional structures of ruderalspecies respond to urbanization and do their shifts follow asimilar pattern along temporal and spatial urbanizationgradients

2 Whatarethekeyunderlyingprocessesieeitherextinction-orcolonization-causedclustering thatdetermine thephylogeneticandfunctionalstructuresofruderalspeciesunderurbanization

2emsp |emspMATERIAL S AND METHODS

21emsp|emspRuderal occurrence data

Toidentifythefloristicchangesofruderalplantspeciesalongspatialandtemporalurbanizationgradientsoccurrencedatawereobtainedfromtwoofourpreviousstudies inShanghaicityandHarbincity(Chenetal2014Tianetal2015) twometropolesexperiencingrapid urbanization in China Both studies indicated that the rud-eral species composition changed significantly along urbanndashruralgradientsThestudy inHarbinalso illustratedthatthephenotypicplasticityhaddecreasedinperennialspeciesbutincreasedinannualspeciesinthepasthalfcentury

Shanghai is located at the edge of the Yangtze River Delta(6340km2insize31deg13prime50PrimeN121deg28prime25PrimeE)wheretheclimateissubtropicalmonsoonwithameanannualtemperatureof178degCandanaverageannualrainfallof14579mmHarbin(10198km2 in size 45deg45prime4808PrimeN126deg38prime5603PrimeE) is locatedon the southeasternedgeoftheSongnenPlainwhichhasatypicalcontinentalmonsoonclimatewith amean annual temperatureof 52degC and an averageannualprecipitationof5691mmBothcitieshavebeenconstructedfromacentralpointandextendradiallyoutwardsfollowingacon-centriccirclepatternwithcharacteristicinnermidandoutercircles

OurtwostudiesusedanidenticalsurveyapproachalongurbanndashruralgradientsEachstudytookthecentralpointofthecityastheoriginandestablished sampling sites in a radialpatternwhichwas

F IGURE 1emspEnvironmentalfiltersandcompetitiveexclusioninfluencethephylogeneticpatternofspeciesassemblyprocessesthroughcolonizationandextinctionCompetitiveexclusionmayalsocausephylogeneticfunctionalclusteringbyexcludinggroupsofecologicallysimilarspecieswithlowcompetitiveabilities(MayfieldampLevine2010)ColonizersmightalsobelessrelatedtoresidentsandthuscauseoverdispersionjustasDarwinproposedinhisnaturalizationhypothesisThewhitecirclerepresentsspecieswithsimilarnicherequirementsandthegrayrhombusrepresentsspecieswithsimilarcompetitiveabilities


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partitioned by the central-suburban ring road At equal radial dis-tancesof1kmateachsiteplotsof1m2wereplacedrandomlyinalltypicalhabitattypes(roadgaps lawnsabandonedlandwithdevel-opedsoilsabandonedlandwithgravelarablelandshrubndashgrasslandgapsforestgapswetlandsandsecondaryforest)Eachinvestigationwasconductedduringthegrowingseason(AprilndashMayinspringandAugustndashSeptember in autumn) In each plot species were identi-fied following theFlora Reipublicae Popularis Sinicae (Flora of China EditorialCommittee2013)Meanwhiletheiroriginswereidentifiedfollowing The Checklist of the Chinese Invasive Plants(Ma2013)Intotal1375plotsinShanghaiand1763plotsinHarbinwereinvestigated

FurthermoreweincludedthehistoricalruderaloccurrencedataofHarbincityrecordedin1955(BaranovGordeevampKuzmin1955)to analyze dynamic shifts across temporal urbanization gradientsBaranovetal(1955)investigatedthesameareaaswedidin2011whichcontainednearlyalltheruderalhabitattypesatthattime(seedetails inChenetal2014)Thedatacontaineda largeamountofinformationwithformostspeciesthescientificnametheChinesenameofthattimeandthehabitatBecausetheplantclassificationsystemsdifferedbetweenthehistoricalandrecentdatawerede-fined the family genus and species of the ruderal vegetation andtransformedall speciesnames intoAPGIII (AngiospermPhylogenyGroup2009)

22emsp|emspPhylogenies and functional traits

WeconstructedphylogenetictreesusingtheonlinetoolPhylomatic(WebbampDonoghue2005)andusedthestoredphylogenetic treeby Zanne etal (2014) to assemble a phylogenetic tree and esti-matebranch lengthsThenwe removedall single-daughternodesusingthefunctionmulti2diinthepackageapeinR(ParadisClaudeampStrimmer2004)Thefinaltreeswereaccuratetothegenusandspecieslevelandprovidedarealisticapproximationoftherealseedplantphylogeny(WebbampDonoghue2005)

Foreachspeciesthatoccurredintheurbanndashruralgradientsofthetwocitieswecollectedfivetraitsthathavebeencommonlyusedinstudiesofplantcommunitiestorepresentresourceparti-tioning differences and resource competition differences (AdlerHillerislambers amp Levine 2007 Duncan etal 2011 ValletDanielBeaujouanRozeacuteampPavoine2010)Specificallythemax-imumplantheightwasused to representaccess to light carbonacquisitionandreproductivestrategiesofspeciesand isdirectlyassociated with the light-competitive ability (Bazzaz Ackerly ampReekie 2000 Westoby Falster Moles Vesk amp Wright 2002)Life forms are used to reflect plantsrsquo adaptive strategies duringseasonswith adverse conditions (EllenbergampMuellerDombois1967) The vegetation formpertains to theplantsrsquo subterraneanorganswhichareassociatedwiththeabilitytocompeteforwaterandnutrients (HayasakaFujiwaraampBox2009)Fruitingtime iscommonlyassociatedwiththevegetativeandreproductiveselec-tionpressuresonthetimingofthedifferentphases(Cornelissenetal 2003) All traitswere recorded from the Flora Reipublicae Popularis Sinicae (Flora of China Editorial Committee 2013) and

Chinese Colored Weed Illustrated Book(ZhangampHirota2000)Lifeformswerecategorizedintothreelevels(summer-annualwinter-annualperennial)Thegrowthformswerecategorizedintoeightlevels (procumbent rosette branched tussock climbinglianapartialrosettepseudorosetteerect)Thefruitingtimewascate-gorizedintofourlevels(springsummerautumnandwinter)Thevegetationformswerecategorizedintofivelevels(widestextentofrhizomatousgrowthmoderateextentnarrowestextentclonalgrowthbystolonsandstruckrootsnon-clonalgrowth)

To explore the evolutionary lability of the traits we usedBlombergsKstatistic(BlombergGarlandampIves2003)totestthephylogeneticsignalofcontinuoustraitsandusedtheldquophylosignaldiscrdquofunction(RezendeLavabreGuimaratildeesJordanoampBascompte2007)toquantifythephylogeneticsignalofothercategoricaltraitsThe significance of the phylogenetic signals was determined bythe rank of the observed relative to the null distribution for 999replications

FurthermoreafunctionaldistancematrixwascreatedusingtheGowerdissimilaritymethod(Gower1971)whichallowsformissingdataandcategoricaldatatorepresentthedissimilarityofspeciesin amultiple-trait space TheGower distancematrix and the un-weighted pair-group clusteringmethod using arithmetic averageswereusedtoconstructatraitdendrograminordertoapplyidenti-calanalyticalmethodstothephylogeneticandtraitdata(PetcheyampGaston 2002) The gowdis and hclust functions in FD package(version10-12)wereusedintheseanalyses(Laliberteacuteetal2014)AllanalyseswereconductedinRversion341(RCoreTeam2017)

23emsp|emspPhylogenetic and functional structure measures

Threespatialsubsets(urbansuburbanandruralareas)inbothcitiesandtwotemporalsubsets(theyears1955amp2011) inHarbinwereextracted based on the historical and survey data in order to ex-aminehowthephylogeneticstructurevariesalongspatiotemporalurbanizationgradientsForeachsubset themeanpairwisephylo-geneticdistance (MPD)ofallpossiblespeciespairswascalculatedto determine the phylogenetic diversity (Webb AckerlyMcPeekampDonoghue2002)Themeanpairwisefunctionaldistance(MFD)wasdeterminedusingthedendrogrammentionedabovetoassessthe variation in the competitive ability of ruderal specieswithur-banizationSubsequentlytheobservedMPDandMFDvalueswerecomparedtotheirrespectiveexpectedvaluesunderanullmodelofrandomcommunityassemblyusingstandardizedeffectsizes (SES)ofMPDandMFDforeachsubsetie

Valuessignificantlymorenegativethanrandomsuggestaphylo-geneticallyclusteredtendencywhilethosesignificantlymoreposi-tivethanrandomindicateanoverdispersedstructure(Webb2000)Becausebothphylogeneticand functionalstructuresaresensitive

MPDSES=

(

observedMPDminusmean of randomMPD)

SD of randomMPD


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tothestatisticalpropertiesofdifferentnullmodels (Hardy2008)weused threedifferentnullmodelsThe taxanullmodelwasob-tainedbyshufflingdistancematrixlabelsacrossalltaxaincludedinthedistancematrixThephylogenynullmodelwascreatedbydraw-ingspeciesfromthepoolofspeciesoccurringinthephylogenypoolwithequalprobabilityTheindependentnullmodelwasestablishedbyrandomizingthecommunitymatrixwith the independentswapalgorithmandwasthestrictestnullmodel(NordenLetcherBoukiliSwensonampChazdon 2012) Thesemetricswere calculated usingthepackagepicanteinRversion341(Kembeletal2010)

24emsp|emspPhylogenetic and functional patterns of species colonization and local extinction

Acrossthetemporalurbanizationgradientswedefinedtheextinctspecies as those that were recorded only in 1955 while colonistspecieswerethosethatwererecordedonlyin2011Residentspe-cieswerethosethatwererecordedinboth1955and2011AcrosstheurbanndashruralgradientswedefinedtheextinctspeciesasthosethatwererecordedonlyintheruralareawhilethecolonistspecieswerethosethatwererecordedonlyinthesuburbanurbanareaandresidentspecieswerethosethatwererecordedinboththeruralandsuburbanurbanareasWefollowedasimilarapproachasthatpro-posedbyLietal (2015)withtwometricsβ-MPD(meanpairwisephylogenetic distance between colonistsextinct species and resi-dents)andβ-MFD(meanpairwisefunctionaldistancebetweencolo-nistsextinctspeciesandresidents)todeterminethemeanpairwisephylogenetic and functional distance between colonistsextinctspeciesandresidents inordertoquantifythesimilaritiesbetweenthecolonistsextinctspeciesandresidentsofeachsubsetNegativeSESvalues indicatethatcolonistsextinctspeciesaremorecloselyrelatedor similar to the residents thanexpectedbychancewhilepositivevaluesindicatetheoppositeWeperformedtheseanalyses

foreachsubsetusingthecomdist and comdistntfunctionsintheRpackagepicante

The shifts in phylogenetic and functional structures along ur-banizationgradientsdonotonlydependontherelatednessofthecolonists and locally extinct species to residents but also on thephylogeneticandfunctionalstructuresof thecolonistsand locallyextinct species Thus we calculated theMPDSES andMFDSES for colonistsand locallyextinct species ineach subsetusing identicalnull models for β-MPDSES(standardizedeffectsizeofMPDbetweencolonistsextinctspeciesandresidents)andβ-MFDSES(standardizedeffectsizeofMFDbetweencolonistsextinctspeciesandresidents)asthosementionedabove

3emsp |emspRESULTS

31emsp|emspChanges in phylogenetic and functional structures

Overall the phylogenetic structures of ruderal species exhibitedclear clustering trends with increasing urbanization both spatiallyandtemporallyThemaximumplantheight(Kvalue04947p lt 001 lambdavalue09717p lt001)andothercategoricaltraitsrevealedsignificantphylogeneticsignal(seedetailsinTable1)

In Harbin city the standardized effect size of mean pairwisephylogeneticdistance(MPDSES)valuesdecreasedfromsignificantlypositive(p lt001)in1955tosignificantlynegative(p lt001Table2)in2011underallthreenullmodelswhichindicatesthatthephylo-genetic structuresof ruderal species clusteredwith increasingur-banizationovertime

Along the urbanndashrural gradients of both cities the MPDSES values were negative (Figure 2 p lt 005) and were increasingly negative when going from rural to urban systems via suburbanareasunderallthreemodelsTheMPDSESvaluewassignificantly

TABLE 1emspTraitsusedintheanalysesandphylogeneticsignalsweretestedbasedontheldquophylosignaldiscrdquofunctionforfourcategoricaltraits(Rezendeetal2007)

Functional traits Data source Missing data

Observed number of changes

Mean null number of changes p Categories

Height FRPSa 8 ndash ndash ndash Continuoustraits

Life forms FRPSaCCWb 0 66 90 0001 Summer-annualWinter-annualPerennial

Fruitingtime FRPSa 4 53 65 0001 SpringSummerAutumnWinter

Vegetationforms CCWb 14 45 56 0001 WidestextentofrhizomatousgrowthModerateextentNarrowestextentClonalgrowthbystolonsandstruckrootsNon-clonalgrowth

Growthforms CCWb 6 68 124 0001 ProcumbentRosetteBranchedTussockClimbingorlianaPartialrosettePseudorosetteErect

Tocheckphylogeneticsignaloffourcategoricaltraitsminimumnumberoftraitstatechangesacrossthephylogenetictreewascomparedtoanullmodelgeneratedbyrandomizingthetraitstatesacrossthetipsofthetree999times(MaddisonampSlatkin1991)Iftheobservedminimumnumberofchangessignificantlylowerthanexpectedmeannullvaluesweconsideredthatrelatedspecieshavesimilartraitstates(presenceofphylogeneticsignal)aFloraReipublicaePopularisSinicaebFloraofChinaandChineseColoredWeedIllustratedBook


CUI et al

negativeintheurbanareasofbothcities(exceptundertheinde-pendentnullmodel) and in theHarbin suburbanareaThese re-sultsdemonstratethatthephylogeneticstructuresalsoclusteredwith increasing spatial urbanization Meanwhile there were nosignificant functional shifts along the spatial urbanization gradi-ents (Figure2) showing that theobservationsofmeanpairwisefunctionaldistance(MFDSES)weresimilartotheexpectationsbychance The only exceptionwas in the Shanghai suburban areawheretheMFDSESwassignificantlynegativeundertheindepen-dentnullmodel(p lt 005)

32emsp|emspPhylogenetic and functional patterns of species colonization and extinction

InHarbincitytheβ-MPDSESofcoloniststoresidentsforthetem-poralgradientwassignificantlynegativeandtheMPDSES of colo-nistswassignificantlynegative indicatingthatcolonistsofcloselyrelated speciesweremore similar to the residents than expectedbychanceInadditiontheβ-MPDSESofextinctspeciestoresidentswassignificantlynegativeforthetemporalgradientwhichindicatesthatextinctspeciesweremoresimilartoresidentsthanexpectedby

TABLE 2emspThetemporalcomparisonofphylogeneticstructuresinHarbinweremeasuredusingthestandardizedeffectsizesofmeanpairwisephylogeneticdistance(MPDSES)withthreenullmodels

Null models Observed MPD Mean of random MPD SD of random MPD MPDSES p value

Richness

1955 295590 291421 1491 2632 1000

2011 257007 291358 7222 minus4597 0001

Phylogeny

1955 295590 291465 1496 2778 1

2011 257007 291492 7342 minus4532 0001

Independent

1955 295590 290973 1548 3041 1

2011 257007 279636 5532 minus4086 0001

ThetaxanullmodelwasobtainedbyshufflingdistancematrixlabelsacrossalltaxaincludedinthedistancematrixThephylogenynullmodelwascre-atedbydrawingspeciesfromthepoolofspeciesoccurringinthephylogenypoolwithequalprobabilityTheindependentnullmodelwasestablishedbyrandomizingthecommunitymatrixwiththeindependentswapalgorithmPositiveMPDSESvaluesindicateoverdispersionandnegativeMPDSES valuesindicateclusteringMPD=MeanpairwisephylogeneticdistanceMPDSES=standardizedeffectsizeofMPDmeansverysignificant(p lt 001)

F IGURE 2emspRuderalphylogenetic(left)andfunctional(right)structuresalongurbanndashruralgradientsThespatialchangesinphylogeneticandfunctionalstructuresinShanghaiandHarbinweremeasuredusingthestandardizedeffectsizesofthemeanpairwisephylogeneticfunctionaldistance(MPDSESMFDSES)usingthreenullmodelsThex-axisindicatestheurbanndashruralgradientsandthey-axisindicatestheresultsunderthethreenullmodelsTheblackcircleindicatesasignificantdifferencefromthatexpectedbychance(p lt005)thewhitecircleindicatesanon-significantdifferencefromthatexpectedbychance(p gt 005)


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chancewhiletheMPDSESofextinctspecieswassignificantlyposi-tiveieindicatingoverdispersion

Along the spatial urbanization gradient of both cities the β- MPDSESofcoloniststoresidentswasnotsignificantlydifferentfromzeroforanypairedgradientHowevertheβ-MPDSESofextinctspe-cies to residentswassignificantlypositivebetweenallpairedgra-dients (Table 3) which indicates that the phylogenetic structuresofextinct speciesweremoredissimilar to thoseof residents thanexpected by chanceOn the other hand the functional structureof ruderal species showed no significant shift towards clusteringor overdispersion along the urbanndashrural gradients The β-MFDSES ofcolonists toresidentswassignificantlynegativefor therural tosuburbanareainShanghaicityandfromtheruraltourbanareainHarbincity(Table3)whichindicatesthatthefunctionalstructuresofcolonistspeciesweremoresimilartothoseofresidentsthanex-pectedbychanceExtinctspecieshadnosignificantfunctionalrela-tionshipwithresidents

4emsp |emspDISCUSSION

Theurbanizationprocessisexpectedtocauselarge-scaleglobalbiotichomogenization (McKinney2006)withbiodiversitybecomingmoresimilaroveraspecifiedtimeintervalduetospeciescolonizationandex-tinction(Earlyetal2016)Thishomogenizationphenomenoncausedbyurbanizationhasalsoledtoadramaticdeclineinphylogeneticrich-ness and divergence in urban floras (Knapp etal 2012) Based ontheseglobalpatternsandinlightoftherapidurbanizationprocessinChinaoverthepasthalfcenturywehypothesizedthatnotonlydidthephylogeneticdiversityofruderalspeciesdeclineinChinesecitiesbuttheirstructuresalsoclusteredwithincreasingurbanizationintensity

By combining the spatiotemporal phylogenetic data of ruderalspeciesourresultsdemonstratethattherewasaclearphylogenetictransition from early overdispersion to later clustering under thetemporalurbanizationprocess inHarbincityMeanwhilephyloge-neticclusteringfromruraltourbanareasalsooccurredinbothcitiesSeveralstudieshaveshownsimilarresultswhenexploringthephy-logeneticorfunctionalpatternsofdifferenttaxa(iebirdsinsectsbats and fish) under urbanization For instance Riedinger et al(2013)reportedthatontheconsideredscale(36km2intheirstudy)batspeciesweremoresimilarthanexpectedfromnullmodelswithanincreaseinanthropogenichabitatsalthoughthespeciesrichnessdecreasedRicottaetal(2015)documentedthatsignificantcluster-ingalsooccurredacrossthephylogenyoftheurbanfloraofBelgium

Our analyses indicated for the first time that both temporalcomparisonandspatialcomparisonapproachescouldshowsimilarclustering patterns with increasing urbanization but that the un-derlying drivers of this clusteringwere different At the temporalscaletheholisticclusteringpatternssuggestthatthesimilaritybe-tweenthecolonistsandresidentsdrovephylogeneticclusteringastheirpredominantroleeventhoughthesimilaritybetweentheex-tinct species and the residents simultaneouslydrovephylogeneticoverdispersionAcrossthespatialgradientshoweverthephyloge-netic clusteringwas primarily driven by the dissimilarity betweenthe extinct species and the residents while the colonists had nosignificanteffectTheseresultssuggestthatthespatialcomparisondoesnotalwaysreflecttheactualprocessesoftemporaldynamicsMoreoveranimportantquestionthatarisesiswhythedriversalongthetemporalversusspatialurbanizationgradientsweresodifferentToanswerthesequestionstheunderlyingmechanismsmaintainingplant diversity across spatial and temporal urbanization gradientsshouldbeexamined

TABLE 3emspPhylogeneticdistancesandfunctionaldissimilaritiesofcolonistsextinctspeciesandresidentsalongtemporalandurbanndashruralgradients

City Gradients Groups Species No

Phylogenetic structure Functional structure

MPDSES

β- MPDSES to residents MFDSES

β- MFDSES to residents

Harbin 1955rarr2011 Colonists 110 minus43493 minus37079 ndash ndash

Extinctspecies 65 27035 minus15481 ndash ndash

Shanghai RrarrS Colonists 30 minus0006 minus02354 0062 minus2710

Extinctspecies 19 09904 23084 00510 03602

RrarrU Colonists 41 minus05073 minus08088 minus00308 04918

Extinctspecies 24 02654 31197 minus09094 minus08545

Harbin RrarrS Colonists 13 00611 00091 00611 04581

Extinctspecies 54 03057 23868 03057 minus03825

RrarrU Colonists 6 minus10150 minus10301 minus24224 minus12642

Extinctspecies 77 minus01270 18476 08170 15256

Thephylogeneticdistancesandfunctionaldissimilaritiesbetweencolonistsextinctspeciesandresidentsweremeasuredusingtheβ-MPDSES and β- MFDSESbasedonLisapproach(Lietal2015)NegativevaluesindicatecolonistsextinctspeciesaremoresimilartotheresidentsthanrandomdrawsfromthespeciespoolwhilepositivevaluessuggesttheoppositeMPDSES=standardizedeffectsizeofMPDMFDSES=standardizedeffectsizeofMFDβ-MPDSES=standardizedeffectsizeofMPDbetweencolonistsextinctspeciesandresidentsβ-MFDSES=standardizedeffectsizeofMFDbe-tweencolonistsextinctspeciesandresidentsmeanssignificant(p lt005)meansverysignificant(p lt 001)


CUI et al

At the temporal scale urbanization causes various habitatchangesegduringthelasthalfcenturyinHarbincitytheannualtemperature showeda significant increasing trendwitha rateof04degC10yearsOf the totalarable land547wasconverted tourban land from1976 to 2010 (Chen etal 2014)Moreover thepopulation increased from1million in the1950s tomore than9millionin2010swhichsignificantlyintensifiedthefrequencyandintensity of disturbance in urban areas Combining our resultswe concluded thatwith rapidurbanizationover time the ruderalspeciesweresuffering fromexposure tohighlystressfulenviron-mentswhichactedasamultifilter selectingruderalspecieswithsuitabletolerancetraitsSpecificallymultiplespecieswithsimilarlysuitabletraitswereselectedforintheimmigrationandextinctionprocesses which caused colonists to becomemore phylogeneti-cally similar to the residents thanbychanceMeanwhile thecol-onistspeciesalsostrengthenedtheintercompetitiverelationshipsamong closely related species and theweaker competitorswereeliminatedby strongerones in theneighboringecological nicheswhich caused the similarity between the extinct species and theresidentsForinstancebecauseofthesimilarecologicalnichesofSolidago canadensis and Solidago decurrensbutstrongercompetitiveabilityofS canadensisS canadensisasan invasivespeciescolo-nized local ecosystems and eliminated the indigenous species S decurrens(DongLuZhangChenampLi2006)

Differently at the spatial scale even though the phylogeneticstructuresalsoshiftedtowardsclusteringwithincreasingurbaniza-tiononlythephylogeneticstructureofextinctspecieswassignifi-cantlydissimilar to thatof the residents andwecouldnotdetectanyphylogeneticsignaturebetweenthecolonistsandtheresidentsTheseresultsdemonstratethatphylogeneticclusteringacrossspa-tial urbanization gradients mainly occurred through species elim-ination processes insteadof immigration processes It thus seemsthatasetofspecieswithunsuitabletraitswasfilteredoutbyabi-oticenvironmentalchangesieenvironmentalfilteringorthatspe-cies groupswith lower competitive abilitieswereexcludedby thestrongeronesiecompetitiveexclusionHoweverintwoofthesecases the colonist species should also be significantlymore simi-lartoresidentsthanbychancewhichwasnotconsistentwithourresults After analyzing the species composition and the origin of

eachspatial subset (Figure3)we inferred that the reason for thisresultwasthatcolonistsintheimmigrationprocessesincludemanyinvasivespeciesthatlacknaturalenemiesinthelocalurbanecosys-temandcanspreadquickly toeveryspatialurbanizationgradientThereforethespatialcomparisonsubstitutionwouldcausebias intermsofreflectingtherealeffectofinvasivespeciesasthecolonistsonthephylogeneticpatternsofthecommunityThetemporal-basedapproacheswerefreefromthisproblembecausethetimeatwhichthespeciesimmigratedhadbeendetermined

Moreover in order to distinguish between the possiblemech-anisms of the extinction processes environmental filtering andcompetitiveexclusionfunctionaltraitswereusedinanattempttodetermine the relative importance of abiotic and biotic processesin driving the community assembly (Mason amp de Bello 2013) Ameta-analysisofthefunctionaltraitsofannualplantsshowedthatdifferences in resource competition could bewell correlatedwithmaximum height phenology seed mass and several other traits(KraftGodoyampLevine2015)Thishypothesisprovidesanunder-standingofthepathwaysthroughwhichcommunityassemblypro-cessesaffectfunctionaltraits(MayfieldampLevine2010)Thereforeweevaluatedthedifferencesincompetitionbasedonthefivecor-relatedfunctionaltraitsweselectedTheresultsdidnotcorrespondwith the expectation that competitive exclusion drove the phylo-genetic and functional clustering through the exclusion of groupsof ecologically similar species with low competitive abilities butdemonstratedthattheurbanizationprocessdidnothavesignificanteffectsonthecompetitiveabilitiesofruderalspeciesattheregionalscale(Table3)Thereforebasedontheassumptionthatthephylo-geneticdistancesamongspeciesareconservativeintermsoftheirfunctional traits andenvironmentalpreferencesoverevolutionarytimetherewasnotsufficientevidencetodemonstrateinourstudythatcompetitiveexclusionwastheprimarymechanismforspeciesclusteringthroughspatialextinctionprocesses

Hencewesuggestthatimmigrationprocessesinurbanareasare the dominant forces across temporal urbanization gradientsinclusteringthephylogeneticstructureofruderalspeciesinlinewithpredictions fromotherstudies (Ricottaetal2009Ricottaetal 2012Čeplovaacute etal 2015) In contrast extinction insteadof the immigrationprocess is theprimarydriverofphylogenetic

F IGURE 3emspVenndiagramillustratingthedistributionpatternofinvasivespeciesineachregion(urbansuburbanandrural)ofHarbin(left)andShanghai(right)thegrayintensityisproportionaltothepercentageMorethan85oftheinvasivespeciesaredistributedinatleasttworegionsalongtheurbanndashruralgradients


CUI et al

clusteringacross spatialurbanizationgradientsAbioticenviron-mental filters representedby stressful environments anddistur-bances in urban areas are the possible mechanisms underlyingsuch clustering by preventing the establishment or persistenceof species in particular habitats Additionally competitive ex-clusionmayalsoplayanoppositerole inthetemporalclusteringprocesseswhichdispersedthephylogeneticstructureofruderalspeciesbylimitingcoexistenceamongcloselyrelatedspeciesbutnot by excluding groups of ecologically similar specieswith lowcompetitiveability(Figure4)

5emsp |emspCONCLUSIONS

Urbanization has profoundly affected facets of diversity in localecosystemsandhascausedbiotichomogenizationamongdifferenturbanareasthroughspeciesimmigrationandextinctionprocessesByusing ruderal species as our selected species group our studyfoundthatthedriversobtainedusingthespatialcomparisonsubsti-tutionapproachdifferedfromthosefoundwiththetemporalcom-parisonapproachHencewesuggestthatthedeficienciesofspatialcomparisonsubstitutionsshouldbeseriouslyconsideredinrelatedstudiesFurtherwespeculatethatbiotichomogenizationwillcon-tinuetointensifywithacceleratedspeciesinvasionsandexpandingurbanizationinthefuture

ACKNOWLEDG EMENTS

WethankDocShao-pengLiwhoprovidedenlightenmentandin-depthideasatthebeginningofouranalyticalworkWeappreciatetherevisionworkforthispaperconductedbyXi-jinZhangandZhi-wenGaoWealsothanktheanonymousrefereesandtheeditorsfortheircommentsonearlierdrafts

DATA ACCE SSIBILIT Y

Therawdatasupportingthefindingsofthisstudyareavailableonfigsharecom(httpsdoiorg106084m9figshare7611743v1)

ORCID

Yi Chong Cui httpsorcidorg0000-0002-2134-2435

Kun Song httpsorcidorg0000-0001-8019-9707

Peter M van Bodegom httpsorcidorg0000-0003-0771-4500

Ying Ji Pan httpsorcidorg0000-0002-8203-3943

R E FE R E N C E S

Adler P HilleRisLambers J amp Levine J M (2007) A nichefor neutrality Ecology Letters 10 95ndash104 httpsdoiorg101111j1461-0248200600996x

AdlerPBampLauenrothWK2003ThepoweroftimespatiotemporalscalingofspeciesdiversityEcology Letters6749ndash756httpsdoiorg101046j1461-0248200300497x

BaranovAGordeevTampKuzminVI(1955)Index florae Harbinensis HarbinChinaHeilongjiangPublishingGroup

BazzazFAAckerlyDDampReekieEG(2000)Reproductivealloca-tioninplantsInMFenner(Ed)Seeds the ecology of regeneration in plant communities(pp1ndash29)WallingfordCTCABIPublishing

BlombergSPGarlandJrTamp IvesAR (2003)Testing forphylo-geneticsignalincomparativedatabehavioraltraitsaremorelabileEvolution 57 717ndash745 httpsdoiorg101111j0014-38202003tb00285x

Boivin N L Zeder M A Fuller D Q Crowther A Larson GErlandsonJMhellipPetragliaMD(2016)Ecologicalconsequencesof human niche construction Examining long-term anthropogenicshaping of global species distributionsProceedings of the National Academy of Sciences of the United States of America1136388ndash6396httpsdoiorg101073pnas1525200113

Bonthoux S Barnagaud J-Y Goulard M amp Balent G (2013)Contrasting spatial and temporal responses of bird communities

F IGURE 4emspTheruderalsortingprocessunderurbanizationattheregionalscale(a)Colonistspecieswithsuitablecompetitiveabilitythatimmigratedintotheurbanareathroughglobaltradeandgardeningpractice(b)Thesespeciesstrengthenedtheintensityofcompetitionamongcloselyrelatedspeciestherebyeliminatinglocalspecieswithlowercompetitiveability(c)Environmentalmodificationincreasesthestrengthofabioticfiltering(egdisturbanceanddroughtstress)therebypreventingcolonizationbyandthepersistenceofunsuitablespeciesWhitecirclesrepresentspecieswithsimilarnicherequirementsandgrayrhombirepresentspecieswithsimilarcompetitiveabilities


CUI et al

to landscape changes Oecologia 172 563ndash574 httpsdoiorg101007s00442-012-2498-2

BrezaLC(2015)A new adaptive landscape urbanization as a strong evo-lutionary forceMasterlsquosthesisUniversityofTennessee

BrunbjergAKBorchseniusFEiserhardtWLEjrnaeligsRampSvenningJ-C (2012)DisturbancedrivesphylogeneticcommunitystructureincoastaldunevegetationJournal of Vegetation Science231082ndash1094httpsdoiorg101111j1654-1103201201433x

ČeplovaacuteNLososovaacuteZZelenyacuteDChytryacuteMDanihelkaJFajmonK hellip Tichyacute L (2015) Phylogenetic diversity of central-EuropeanurbanplantcommunitieserffectsofalienspeciesandhabitattypesPreslia871ndash16

ChaveJChustGampTheacutebaudC (2007)The importanceofphylo-geneticstructureinbiodiversitystudiesInDStorchampPMarquet(ERds)Scaling Biodiversity(pp151ndash167)CambridgeUKCambridgeUniversity Press httpsdoiorg101017cbo9780511814938 010

ChenXWangWLiangHLiuXampDaL(2014)Dynamicsofrud-eralspeciesdiversityundertherapidurbanizationoverthepasthalfcenturyinHarbinNortheastChinaUrban Ecosystems17455ndash472httpsdoiorg101007s11252-013-0338-8

CollinghamYCampHuntley B (2000) Impacts of habitat fragmenta-tionandpatchsizeuponmigrationratesEcological Applications10131ndash144httpsdoiorg1023072640991

Cornelissen J H C Lavorel S Garnier E Diacuteaz S Buchmann NGurvichD Ehellip PoorterH (2003) A handbook of protocols forstandardised and easy measurement of plant functional traitsworldwide Australian Journal of Botany 51 335ndash380 httpsdoiorg101071bt02124

CurritNampEasterlingWE(2009)Globalizationandpopulationdriversofrural-urbanland-usechangeinChihuahuaMexicoLand Use Policy26535ndash544httpsdoiorg101016jlandusepol200808001

DiacuteazSampCabidoM(2001)Viveladiffeacuterenceplantfunctionaldiver-sitymatterstoecosystemprocessesTrends in Ecology amp Evolution16646ndash655httpsdoiorg101016s0169-5347(01)02283-2

DongM Lu J ZhangW Chen J amp Li B (2006) Canada golden-rod (Solidago canadensis) An invasive alien weed rapidly spread-ing in China Acta Phytotaxonomica Sinica 44 72ndash85 httpsdoiorg101360aps050068

Duncan R P Clemants S E Corlett R T Hahs A K McCarthyM A McDonnell M J hellip Williams N S G (2011) Planttraits and extinction in urban areas a meta-analysis of 11 cit-ies Global Ecology and Biogeography 20 509ndash519 httpsdoiorg101111j1466-8238201000633x

EarlyRBradleyBADukesJSLawlerJJOldenJDBlumenthalDMhellipTatemAJ(2016)Globalthreatsfrominvasivealienspeciesinthetwenty-firstcenturyandnationalresponsecapacitiesNature Communications712485httpsdoiorg101038ncomms12485

EllenbergHampMuellerDomboisD(1967)AkeytoRaunkiaerplantlifeformswithrevisedsubdivisionsBerichte des Geobotanischen Instituts ETH Stiftung Ruumlbel3756ndash73

FloraofChinaEditorialCommittee(Eds)(2013)Flora of ChinaBeijingChinaSciencePressandStLouisMOMissouriBotanicalGardenPress

FukamiTampWardleDA(2005)Long-termecologicaldynamicsrecip-rocalinsightsfromnaturalandanthropogenicgradientsProceedings of the Royal Society B Biological Sciences2722105ndash2115httpsdoiorg101098rspb20053277

Gower J C (1971) A general coefficient of similarity and some ofits properties Biometrics 27 857ndash871 httpsdoiorg102307 2528823

HardyO J (2008)Testing the spatial phylogenetic structureof localcommunities statisticalperformancesofdifferentnullmodelsandteststatisticsonalocallyneutralcommunityJournal of Ecology96914ndash926httpsdoiorg101111j1365-2745200801421x

HautierYTilmanD IsbellFSeabloomEWBorerETampReichP B (2015) Anthropogenic environmental changes affect ecosys-tem stability via biodiversity Science 348 336ndash340 httpsdoiorg101126scienceaaa1788

HayasakaDFujiwaraKampBoxEO(2009)RecoveryofsandybeachandmaritimeforestvegetationonPhuketIsland(Thailand)afterthemajorIndianOceantsunamiof2004Applied Vegetation Science12211ndash224httpsdoiorg101111j1654-109x200901017x

HilleRisLambersJ(2015)ExtinctionrisksfromclimatechangeScience348501ndash502httpsdoiorg101126scienceaab2057

HopeDGriesCZhuWFaganWFRedmanCLGrimmNBhellip Kinzig A (2003) Socioeconomics drive urban plant diversityProceedings of the National Academy of Sciences of the United States of America1008788ndash8892httpsdoiorg101073pnas1537557100

IvesCDLentiniPEThrelfallCGIkinKShanahanDFGarrardGEhellipKendalD(2016)CitiesarehotspotsforthreatenedspeciesGlobal Ecology amp Biogeography25117ndash126httpsdoiorg101111geb12404

JohnsonALTauzerECampSwanCM(2015)Humanlegaciesdif-ferentiallyorganize functionalandphylogeneticdiversityofurbanherbaceous plant communities at multiple spatial scales Applied Vegetation Science18513ndash527httpsdoiorg101111avsc12155

KembelSWCowanPDHelmusMRCornwellWKMorlonHAckerlyDDhellipWebbCO(2010)PicanteRtoolsforintegratingphylogeniesandecologyBioinformatics261463ndash1464httpsdoiorg101093bioinformaticsbtq166

KeshtkarHampVoigtW(2016)Potential impactsofclimateandland-scape fragmentation changes on plant distributions Couplingmulti-temporal satellite imagery with GIS-based cellular automatamodel Ecological Informatics32145ndash155httpsdoiorg101016jecoinf201602002

Knapp S Dinsmore L Fissore C Hobbie S E Jakobsdottir IKattge J hellip Cavender-Bares J (2012) Phylogenetic and func-tional characteristics of household yard floras and their changesalong an urbanization gradient Ecology 93 S83ndashS98 httpsdoiorg10189011-03921

KnappSKuumlhnISchweigerOampKlotzS(2008)Challengingurbanspecies diversity contrasting phylogenetic patterns across plantfunctional groups in Germany Ecology Letters 11 1054ndash1064httpsdoiorg101111j1461-0248200801217x

KnappSKuumlhnIStolleJampKlotzS(2010)ChangesinthefunctionalcompositionofaCentralEuropeanurbanfloraoverthreecenturiesPerspectives in Plant Ecology Evolution and Systematics12235ndash244httpsdoiorg101016jppees200911001

KnappSWinterMampKlotzS(2017)Increasingspeciesrichnessbutdecreasing phylogenetic richness and divergence over a 320-yearperiod of urbanization Journal of Applied Ecology 54 1152ndash1160httpsdoiorg1011111365-266412826

KraftNJBGodoyOampLevineJM(2015)PlantfunctionaltraitsandthemultidimensionalnatureofspeciescoexistenceProceedings of the National Academy of Sciences of the United States of America112797ndash802httpsdoiorg101073pnas1413650112

LaliberteacuteELegendrePampShipleyB(2014)FDmeasuringfunctionaldiversityfrommultipletraitsandothertoolsforfunctionalecologyR package version 10-12 Retrieved from httpsCRANR projectorgpackage=FD

LiSCadotteMWMeinersSJHuaZJiangLampShuW(2015)Species colonisation not competitive exclusion drives communityoverdispersionoverlong-termsuccessionEcology Letters18964ndash973httpsdoiorg101111ele12476

MaJS(2013)The Checklist of Chinese invasive speciesBeijingChinaHighEducationPress

MackRNampLonsdaleWM(2001)Humansasglobalplantdispers-ersGettingmore thanwebargained forCurrent introductionsofspecies foraestheticpurposespresent the largest singlechallenge


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for predicting which plant immigrants will become future pestsBioScience5195ndash102httpsdoiorg1016410006-3568(2001)051[0095hagpdg]20co2

MaddisonWPampSlatkinM(1991)Nullmodelsforthenumberofevo-lutionarysteps inacharacteronaphylogenetictreeEvolution451184ndash1197httpsdoiorg101111j1558-56461991tb04385x

MasonNWHampdeBello F (2013) Functional diversity a tool foranswering challenging ecological questions Journal of Vegetation Science24777ndash780httpsdoiorg101111jvs12097

MayfieldMMampLevineJM(2010)Opposingeffectsofcompetitiveex-clusiononthephylogeneticstructureofcommunitiesEcology Letters131085ndash1093httpsdoiorg101111j1461-0248201001509x

McDonnellM JPickettSTAGroffmanPBohlenPPouyatRVZippererWChellipMedleyK(1997)Ecosystemprocessesalonganurban-to-ruralgradientUrban Ecosystems121ndash36httpsdoiorg101023a1014359024275

McGillBJEnquistBJWeiherEampWestobyM(2006)Rebuildingcommunity ecology from functional traits Trends in Ecology amp Evolution21178ndash185httpsdoiorg101016jtree200602002

McKinneyML(2002)UrbanizationbiodiversityandconservationTheimpactsofurbanizationonnativespeciesarepoorlystudiedbutedu-catingahighlyurbanizedhumanpopulationabouttheseimpactscangreatlyimprovespeciesconservationinallecosystemsBioScience52883ndash890 httpsdoiorg1016410006-3568(2002)052[0883ubac]20co2

McKinney M L (2006) Urbanization as a major cause of biotic ho-mogenization Biological Cconservation 127 247ndash260 httpsdoiorg101016jbiocon200509005

McKinneyML (2008)EffectsofurbanizationonspeciesrichnessAreviewofplantsandanimalsUrban Ecosystems11161ndash176httpsdoiorg101007s11252-007-0045-4

NordenN Letcher S G Boukili V SwensonN G amp Chazdon R(2012)Demographicdriversofsuccessionalchangeinphylogeneticstructureacrosslife-historystagesinplantcommunitiesEcology93S70ndashS82httpsdoiorg10189010-21791

Palma E Catford J A Corlett R T Duncan R P Hahs A KMcCarthyMAhellipVesk PA (2017) Functional trait changes intheflorasof11citiesacrosstheglobeinresponsetourbanizationEcography40875ndash886httpsdoiorg101111ecog02516

Paradis E Claude J amp Strimmer K (2004) APE analyses of phylo-genetics and evolution inR languageBioinformatics20 289ndash290httpsdoiorg101093bioinformaticsbtg412

PetcheyOLampGastonKJ(2002)Functionaldiversity(FD)speciesrichness and community compositionEcology Letters5 402ndash411httpsdoiorg101046j1461-0248200200339x

Piano E DeWolf K Bona F Bonte D Bowler D E IsaiaM hellipHendrickxF(2016)Urbanizationdrivescommunityshiftstowardsthermophilic and dispersive species at local and landscape scalesGlobal Change Biology232554ndash2564

PriceSJDorcasMEGallantALKlaverRWampWillsonJD(2006)ThreedecadesofurbanizationEstimatingtheimpactofland-coverchange on stream salamander populationsBiological Conservation133436ndash441httpsdoiorg101016jbiocon200607005

RCoreTeam(2017)R A language and environment for statistical comput-ingViennaAustriaRFoundationforStatisticalComputing

RezendeELLavabreJEGuimaratildeesPRJordanoPampBascompteJ (2007) Non-random coextinctions in phylogenetically struc-tured mutualistic networks Nature 448 925ndash928 httpsdoiorg101038nature05956

RicottaCGodefroidSHeathfieldDampMazzoleniS(2015)Limitedevidence of local phylogenetic clustering in the urban flora ofBrussels Plant Biosystems14931ndash37httpsdoiorg101080112635042013809029

RicottaCHeathfieldDGodefroidSampMazzoleniS(2012)Theef-fectsofhabitatfilteringonthephylogeneticstructureoftheurbanflora of Brussels (Belgium) Community Ecology1397ndash101httpsdoiorg101556comec132012112

Ricotta C La Sorte F A Pyšek P Rapson G L Celesti-Grapow L amp Thompson K (2009) Phyloecology of urbanalien floras Journal of Ecology 97 1243ndash1251 httpsdoiorg101111j1365-2745200901548x

RiedingerVMuumlllerJStadlerJampBrandlR(2013)Phylogeneticdi-versityofbatsdecreases inurbanenvironmentsBasic and Applied Ecology1474ndash80

Tian Z Song K ampDa L (2015) Distribution patterns and traits ofweedcommunitiesalonganurbanndashruralgradientunderrapidurban-izationinShanghaiChinaWeed Biology and Management1527ndash41httpsdoiorg101111wbm12062

ValletJDanielHBeaujouanVRozeacuteFampPavoineS(2010)Usingbiological traits to assess howurbanization filters plant species ofsmall woodlands Applied Vegetation Science13 412ndash424 httpsdoiorg101111j1654-109x201001087x

Vitousek P M Mooney H A Lubchenko J amp Melillo J M(1997)Human domination of Earths ecosystems Science 277494ndash499

WebbCO(2000)Exploringthephylogeneticstructureofecologicalcommunitiesanexample for rain forest treesAmerican Naturalist156145ndash155httpsdoiorg101086303378

WebbCOAckerlyDDMcPeekMAampDonoghueMJ(2002)Phylogenies and community ecology Annual Review of Ecology and Systematics 33 475ndash505 httpsdoiorg101146annurevecolsys33010802150448

WebbCOampDonoghueM J (2005)Phylomatic treeassembly forappliedphylogeneticsMolecular Ecology Notes5181ndash183

WestobyMFalsterDSMolesATVeskPAampWrightIJ(2002)Plantecologicalstrategiessomeleadingdimensionsofvariationbe-tween speciesAnnual Review of Ecology and Systematics33 125ndash159httpsdoiorg101146annurevecolsys33010802150452

WorldHealthOrganizationampUN-Habitat(2016)Global report on urban health equitable healthier cities for sustainable developmentGenevaSwitzerlandWorldHealthOrganization

YannelliFAKochC Jeschke JMampKollmann J (2017)LimitingsimilarityandDarwinsnaturalizationhypothesisunderstandingthedriversofbioticresistanceagainstinvasiveplantspeciesOecologia183775ndash784httpsdoiorg101007s00442-016-3798-8

ZanneAETankDCCornwellWKEastmanJMSmithSAFitzJohnRGhellipOrdonezA(2014)ThreekeystotheradiationofangiospermsintofreezingenvironmentsNature506(7486)89ndash92httpsdoiorg101038nature12872

ZhangZPampHirotaS (2000)Chinese Colored Weed Illustrated Book PR China Institute for the Control of Agrochemicals Ministryof Agriculture and the Japan Association for Advancement ofPhyto-Regulators

How to cite this articleCuiYCSongKGuoXYetalPhylogeneticandfunctionalstructuresofplantcommunitiesalongaspatiotemporalurbanizationgradientEffectsofcolonizationandextinctionJ Veg Sci 201930341ndash351 httpsdoiorg101111jvs12724

J Veg Sci 201930341ndash351 wileyonlinelibrarycomjournaljvs emsp|emsp341

Journal of Vegetation Science

copy 2019 International Association for Vegetation Science

Received7February2018emsp |emsp Revised3December2018emsp |emsp Accepted20December2018DOI101111jvs12724

R E S E A R C H A R T I C L E

Phylogenetic and functional structures of plant communities along a spatiotemporal urbanization gradient Effects of colonization and extinction

Yi Chong Cui12 emsp| Kun Song12 emsp| Xue Yan Guo12emsp| Peter M van Bodegom3 emsp| Ying Ji Pan3 emsp| Zhi Hui Tian4emsp| Xiao Shuang Chen5emsp| Jie Wang12emsp| Liang Jun Da12

1Shanghai Key Lab for Urban Ecological ProcessesandEco-RestorationSchoolofEcologicalandEnvironmentalSciencesEastChinaNormalUniversityShanghaiChina2InstituteofEco-ChongmingShanghaiChina3InstituteofEnvironmentalSciences(CML)LeidenUniversityLeidenTheNetherlands4Eco-EnvironmentalProtectionResearchInstituteShanghaiAcademyofAgriculturalSciencesShanghaiChina5CollegeofMaterialsScienceandEngineeringDonghuaUniversityShanghaiChina

CorrespondenceKunSongandLiangJunDaShanghaiKeyLab for Urban Ecological Processes and Eco-RestorationSchoolofEcologicalandEnvironmentalSciencesEastChinaNormalUniversityShanghaiChinaEmails ksongdesecnueducn ljdadesecnueducn

Funding information ThisworkwassupportedbytheNationalNaturalScienceFoundationofChina(projectNo31770468)SpecialFoundationforStateMajor Basic Research Program of China (2015FY210200-4)ScienceandTechnologyCommissionofShanghaiMunicipality(18DZ120460018295810400)

Co-ordinatingEditorIngolfKuumlhn

AbstractQuestion Urbanizationhasremarkableimpactsonthephylogeneticandfunctionalstructuresofplant communitiesBoth temporal and spatial comparisonsalongur-banizationgradientsarewidelyusedinrelatedstudiesbuttherehasbeenalackofconsistencyintheresultsMoreoverthereisaneedforstudiesthatdeterminespe-ciesassemblymechanismsthroughimmigrationandextinctionThereforetwoques-tions were addressed (a) How do the phylogenetic and functional structures ofruderalspeciesrespondtourbanizationanddotheirshiftsfollowasimilarpatternalongtemporalandspatialurbanizationgradients(b)Whatarethekeyunderlyingprocesses ieeitherextinction-orcolonization-causedclustering thatdeterminethephylogeneticandfunctionalstructuresofruderalspeciesunderurbanizationStudy site Twometropoles(ShanghaiandHarbin)experiencingrapidurbanizationinChinaMethods Wecollectedoccurrencedataonruderalspeciesfrom1955andthepresentintwocitiesStandardizedeffectsizesofmeanpairwisephylogeneticdistanceandofmeanpairwisefunctionaldistancevalues(MPDSESandMFDSESresp)werecalculatedtotestwhethertherewasphylogeneticandorfunctionalstructureclusteringalongspatialortemporalurbanizationgradientsβ-MPDSES and β-MFDSES values were used toquantifythesimilaritiesamongcolonistsextinctspeciesandresidentsResults AlongboththespatialandtemporalgradientstheMPDSES values in each citydecreasedfromsignificantlypositivetosignificantlynegativewithincreasingur-banizationInconsistentlyalongthetemporalgradientstheβ-MPDSESvaluesofthecolonistsextinctspeciestotheresidentsweresignificantlynegativealongthespa-tialgradientstheβ-MPDSESvaluesofextinctspeciestoresidentsweresignificantlypositivewithincreasingurbanizationConclusions Wefoundtherewasaclearphylogeneticclusteringofruderalspecieswith increasing spatial and temporal urbanization gradients Our analysis showedthatthechangesacrosstheurbanndashruralgradientaremainlydrivenbyspeciesgoingextinct that are phylogenetically dissimilar to the resident species The temporal


CUI et al









K E Y W O R D S



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MPDSES=

(


SD of randomMPD


CUI et al






3emsp |emspRESULTS
















CUI et al






Richness

1955 295590 291421 1491 2632 1000

2011 257007 291358 7222 minus4597 0001

Phylogeny

1955 295590 291465 1496 2778 1

2011 257007 291492 7342 minus4532 0001

Independent

1955 295590 290973 1548 3041 1

2011 257007 279636 5532 minus4086 0001




CUI et al










MPDSES






Extinctspecies 19 09904 23084 00510 03602









CUI et al








CUI et al




ACKNOWLEDG EMENTS




ORCID





R E FE R E N C E S










CUI et al





































CUI et al



































CUI et al









K E Y W O R D S



CUI et al












CUI et al












MPDSES=

(


SD of randomMPD


CUI et al






3emsp |emspRESULTS
















CUI et al






Richness

1955 295590 291421 1491 2632 1000

2011 257007 291358 7222 minus4597 0001

Phylogeny

1955 295590 291465 1496 2778 1

2011 257007 291492 7342 minus4532 0001

Independent

1955 295590 290973 1548 3041 1

2011 257007 279636 5532 minus4086 0001




CUI et al










MPDSES






Extinctspecies 19 09904 23084 00510 03602









CUI et al








CUI et al




ACKNOWLEDG EMENTS




ORCID





R E FE R E N C E S










CUI et al





































CUI et al



































CUI et al












CUI et al












MPDSES=

(


SD of randomMPD


CUI et al






3emsp |emspRESULTS
















CUI et al






Richness

1955 295590 291421 1491 2632 1000

2011 257007 291358 7222 minus4597 0001

Phylogeny

1955 295590 291465 1496 2778 1

2011 257007 291492 7342 minus4532 0001

Independent

1955 295590 290973 1548 3041 1

2011 257007 279636 5532 minus4086 0001




CUI et al










MPDSES






Extinctspecies 19 09904 23084 00510 03602









CUI et al








CUI et al




ACKNOWLEDG EMENTS




ORCID





R E FE R E N C E S










CUI et al





































CUI et al



































CUI et al












MPDSES=

(


SD of randomMPD


CUI et al






3emsp |emspRESULTS
















CUI et al






Richness

1955 295590 291421 1491 2632 1000

2011 257007 291358 7222 minus4597 0001

Phylogeny

1955 295590 291465 1496 2778 1

2011 257007 291492 7342 minus4532 0001

Independent

1955 295590 290973 1548 3041 1

2011 257007 279636 5532 minus4086 0001




CUI et al










MPDSES






Extinctspecies 19 09904 23084 00510 03602









CUI et al








CUI et al




ACKNOWLEDG EMENTS




ORCID





R E FE R E N C E S










CUI et al





































CUI et al



































CUI et al






3emsp |emspRESULTS
















CUI et al






Richness

1955 295590 291421 1491 2632 1000

2011 257007 291358 7222 minus4597 0001

Phylogeny

1955 295590 291465 1496 2778 1

2011 257007 291492 7342 minus4532 0001

Independent

1955 295590 290973 1548 3041 1

2011 257007 279636 5532 minus4086 0001




CUI et al










MPDSES






Extinctspecies 19 09904 23084 00510 03602









CUI et al








CUI et al




ACKNOWLEDG EMENTS




ORCID





R E FE R E N C E S










CUI et al





































CUI et al



































CUI et al






Richness

1955 295590 291421 1491 2632 1000

2011 257007 291358 7222 minus4597 0001

Phylogeny

1955 295590 291465 1496 2778 1

2011 257007 291492 7342 minus4532 0001

Independent

1955 295590 290973 1548 3041 1

2011 257007 279636 5532 minus4086 0001




CUI et al










MPDSES






Extinctspecies 19 09904 23084 00510 03602









CUI et al








CUI et al




ACKNOWLEDG EMENTS




ORCID





R E FE R E N C E S










CUI et al





































CUI et al



































CUI et al










MPDSES






Extinctspecies 19 09904 23084 00510 03602









CUI et al








CUI et al




ACKNOWLEDG EMENTS




ORCID





R E FE R E N C E S










CUI et al





































CUI et al



































CUI et al








CUI et al




ACKNOWLEDG EMENTS




ORCID





R E FE R E N C E S










CUI et al





































CUI et al



































CUI et al




ACKNOWLEDG EMENTS




ORCID





R E FE R E N C E S










CUI et al





































CUI et al



































CUI et al





































CUI et al



































CUI et al


































Documents

Phylogenetic and functional structures of plant